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St. John's

$563+ Cheap flights from Colorado to St. John's (ANU)

This is the cheapest round-trip flight price found by a Cheapflights user in the last 72 hours by searching for a flight departing on 2/25. Fares are subject to change and may not be available on all flights or dates of travel.
DEN — ANU
Oct 14 — Oct 211
Tue 10/14
Tue 10/21
1 adult, Economy
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Cheap flight deals from Colorado to St. John's

Keep the following information in mind while searching for Colorado to St. John's flight deals. Data was last updated September 14, 2025.

Round-trip from

$563
(Expedia)

Popular in

December

Cheapest in

November

Average price

$777
From Colorado to St. John's V.C. Bird Intl
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High demand for flights, 0% potential price rise
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Cheapest flight prices on average. 2% potential price decrease ($23 potential savings vs. average RT price).
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Average for round-trip flights in September 2025
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Find flight deals from Colorado to St. John's

Cheapest flights from Colorado to St. John's
Explore the most affordable flight options available from Colorado to St. John's. Find the lowest fares from popular airlines and budget airlines, with prices last updated on September 14, 2025.

This American Airlines deal was found by Cheapflights users on 9/13. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Mon 10/2711:59 pmDEN - ANU
1 stop11h 52mAmerican Airlines
Wed 11/52:15 pmANU - DEN
1 stop10h 33mAmerican Airlines
Deal found 9/13$699
This American Airlines deal was found by Cheapflights users on 9/13. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Thu 11/64:10 pmDEN - ANU
2 stops21h 36mAmerican Airlines
Sun 11/162:15 pmANU - DEN
2 stops25h 22mAmerican Airlines
Deal found 9/13$708
This American Airlines deal was found by Cheapflights users on 9/12. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Mon 11/108:50 amDEN - ANU
1 stop28h 56mAmerican Airlines
Tue 11/185:47 pmANU - DEN
2 stops23h 08mAmerican Airlines
Deal found 9/12$720
This American Airlines deal was found by Cheapflights users on 9/13. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Thu 11/204:45 pmDEN - ANU
2 stops17h 30mAmerican Airlines
Mon 11/242:15 pmANU - DEN
2 stops22h 08mAmerican Airlines
Deal found 9/13$743
This American Airlines deal was found by Cheapflights users on 9/13. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Tue 11/118:50 amDEN - ANU
1 stop28h 56mAmerican Airlines
Sun 11/162:15 pmANU - DEN
2 stops23h 11mAmerican Airlines
Deal found 9/13$766
This American Airlines deal was found by Cheapflights users on 9/11. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sun 11/97:00 amMTJ - ANU
2 stops27h 15mAmerican Airlines
Thu 11/135:47 pmANU - MTJ
2 stops28h 32mAmerican Airlines
Deal found 9/11$927
This American Airlines deal was found by Cheapflights users on 9/11. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sat 12/62:23 pmDRO - ANU
2 stops20h 49mAmerican Airlines
Wed 12/106:00 pmANU - DRO
2 stops27h 24mAmerican Airlines
Deal found 9/11$927
This American Airlines deal was found by Cheapflights users on 9/11. Clicking the “Pick Dates” button in this card will allow you to select your dates and further customize your flight criteria. From there, click “Find deals”, make sure American Airlines is selected, and click “Compare selected” under the list of providers to see comparable flight deals.
Sat 12/65:30 amGJT - ANU
2 stops29h 42mAmerican Airlines
Wed 12/106:00 pmANU - GJT
2 stops24h 56mAmerican Airlines
Deal found 9/11$927

Cheapflights Fare Finder

 
Customize your flight search to find flights from Colorado to St. John's that fit within your specific budget. Explore options based on user searches and filter the results based on your desired price range. Find flights that match your budget for a cost-effective journey. Over the last 7 days, Cheapflights users made 2,558,603 searches. Data last updated September 14, 2025.
Use the filters below to find and compare flights from Colorado to St. John's that are best for you.

Fly from

Colorado

Fly to

St. John's

Route

Depart

Return

Price

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Wed 2/25

10:44 pm-2:09 pm

1 stop12h 25m

St. John's V.C. Bird Intl

Mon 3/2

3:15 pm-8:45 am

1 stop20h 30m

$563

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 2/5

11:14 pm-2:39 pm

1 stop12h 25m

St. John's V.C. Bird Intl

Sun 2/15

3:15 pm-8:45 am

1 stop20h 30m

$687

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Mon 10/27

6:51 pm-12:09 pm

2 stops15h 18m

St. John's V.C. Bird Intl

Wed 11/5

2:15 pm-9:31 am

2 stops22h 16m

$703

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Wed 2/25

4:54 pm-2:05 pm

2 stops18h 11m

St. John's V.C. Bird Intl

Mon 3/2

5:15 pm-9:26 am

2 stops19h 11m

$703

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Mon 11/10

6:52 pm-1:15 pm

2 stops15h 23m

St. John's V.C. Bird Intl

Tue 11/18

5:47 pm-1:55 pm

2 stops23h 08m

$703

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 11/6

4:10 pm-4:46 pm

2 stops21h 36m

St. John's V.C. Bird Intl

Sun 11/16

2:15 pm-12:37 pm

2 stops25h 22m

$708

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 2/5

11:59 pm-4:20 pm

2 stops13h 21m

St. John's V.C. Bird Intl

Sun 2/15

5:15 pm-9:26 am

2 stops19h 11m

$708

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Fri 3/13

11:59 pm-12:52 pm

1 stop10h 53m

St. John's V.C. Bird Intl

Thu 3/19

3:05 pm-11:54 pm

1 stop10h 49m

$724

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Sat 1/10

3:08 pm-12:56 pm

2 stops18h 48m

St. John's V.C. Bird Intl

Sat 1/17

5:10 pm-8:10 am

2 stops18h 00m

$728

DenverSt. John's

DEN - ANU

DENANU

Denver Intl

Thu 11/20

4:45 pm-1:15 pm

2 stops17h 30m

St. John's V.C. Bird Intl

Mon 11/24

2:15 pm-9:23 am

2 stops22h 08m

$743

Flights are sorted by cheapest round-trip flights first.

Deals found on 9/13

Showing 1-10 of 15 results
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Best time to book a flight from Colorado to St. John's

Have a flexible travel schedule? Discover the best time to fly to St. John's from Colorado with our price prediction graph.
Estimated round-trip price
Rates are based on past data. Find the cheapest month and day to book your flight based on your travel requirements, then search for cheap deals.

Cheapflights Insights

Everything you need to know about your flight from Colorado to St. John's

What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

Currently, August is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $500). Flying from Colorado to St. John's, Saint John in June is currently the most expensive (average of $651). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

What is the cheapest time of day to fly from CO to ANU?

Find hourly flight availability from Colorado to St. John's. Discover flight options and departure times throughout the day, allowing you to choose a departure time that suits your schedule. Data last updated September 14, 2025.

When flying from Colorado to St. John's, Saint John, the time of day you decide to fly out makes little to no difference towards the overall price you’ll pay on tickets.

Related info for your journey

Find useful and relevant information for your journey from Colorado to St. John's. Access travel guides, tips, and recommendations to enhance your travel experience. Get information about local attractions, weather, transportation options, and more.

  • What airport do you fly into for flights to St. John's from Colorado?

    If you book a flight to St. John's from Colorado, you will be flying to V.C. Bird Intl, which is the city’s only airport. St. John's V.C. Bird Intl (ANU) is located 3.8 mi from the center of St. John's.

  • How long is the flight from Colorado to St. John's, Saint John?

    A quick flight from Colorado to St. John's, Saint John can take about 12h 25m. JetBlue provides one of the quickest options available for as low as $563. The distance from Colorado to St. John's, Saint John is about 2998 mi. This flight may include one or multiple stops.

  • What are the most popular routes from Colorado to St. John's, Saint John?

    The most popular flight routes from Colorado to St. John's, Saint John are Denver Intl - St. John's V.C. Bird Intl, Grand Junction Regnl - St. John's V.C. Bird Intl and Durango La Plata County - St. John's V.C. Bird Intl.

  • Can I find deals for flights from Colorado to St. John's that include hotel bookings?

    Yes. In addition to deals on Colorado to St. John's flights, Cheapflights offers vacation packages that include both flights and hotel.

  • How can I find direct flights from Colorado to St. John's?

    After entering your origin and destination, apply the non-stop filter on the search result page to find direct flights from Colorado to St. John's.

  • Can I find deals for business class flights from Colorado to St. John's?

    Yes. Cheapflights offers flight deals from Colorado to St. John's by cabin class. In addition to browsing deals, you can also filter by cabin class on the search results page after making a search.

  • What is the cheapest month to book a flight from Colorado to St. John's, Saint John?

    Currently, August is the cheapest month in which you can book a flight from Colorado to St. John's, Saint John (average of $500). Flying from Colorado to St. John's, Saint John in June is currently the most expensive (average of $651). There are several factors that can impact the price of a flight, so comparing airlines, departure airports and flight times can provide users with more options.

See more FAQs

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Alternative routes for Colorado to St. John's

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Top 2 airlines flying from Colorado to St. John's

Discover the top 2 airlines that operate flights from Colorado to St. John's. Compare their services, reliability, and customer satisfaction ratings to choose the airline that best suits your travel preferences and needs. Over the last 7 days, Cheapflights users made 2,558,603 searches. Data last updated September 14, 2025.
AirlineCheapestAverageFlexibilityOn-time
JetBlueCheapest$471Average$679FlexibilityNo cancel feeOn-time62%
American AirlinesCheapest$575Average$804FlexibilityNo cancel feeOn-time71%

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